EVALUATION OF FOOD AZO DYES IN TERMS OF MALE REPRODUCTIVE TOXICITY

Yıl 2024, Cilt: 48 Sayı: 3, 1236 - 1247, 10.09.2024

Büşra Korkut Çelikateş , Merve Baysal

https://doi.org/10.33483/jfpau.1481724

Öz

Objective: Synthetic food dyes are one of the important ingredients that enhance the appearance and taste of industrial and commercial products. However, concerns exist about their potential harm to human health due to their chemical structures, which often contain azo functional groups and aromatic rings. Many studies have stated that dyes belonging to the azo group are nitro derivatives that can cause hypersensitivity reactions, and that the metabolites produced by intestinal microflora are the focus of mutagenesis and carcinogenesis studies. Various studies have shown that azo dyes have negative effects on the male reproductive system, especially on sperm parameters. These effects were accompanied by a decrease in serum testosterone concentration.
Result and Discussion: The increasing interest in studies on food azo dyes has brought about the need to elucidate possible toxicity mechanisms. In this review, general information about commonly used food azo dyes is presented and the results of in vivo studies on their negative effects on the male reproductive system are evaluated.

Anahtar Kelimeler

Food azo dyes, male reproductive system, toxicity

GIDA AZO BOYALARININ ERKEK REPRODÜKTİF TOKSİSİTESİ YÖNÜNDEN DEĞERLENDİRİLMESİ

Öz

Amaç: Sentetik gıda boyaları, endüstriyel ve ticari ürünlerin görünümünü iyileştiren ve lezzetini artıran önemli bileşenlerden biridir. Ancak, çoğunlukla azo fonksiyonel gruplar ve aromatik halkalar içeren kimyasal yapılarından dolayı, bu maddelerin insan sağlığına potansiyel olarak zararlı olabileceği konusunda endişeler bulunmaktadır. Birçok çalışma, azo grubuna dahil olan boyaların aşırı duyarlılık reaksiyonlarına neden olabilen nitro türevleri olduğunu, bağırsak mikroflorası tarafından oluşan metabolitlerin mutajenez ve karsinojenez çalışmalarının odak noktasında yer aldığını belirtmiştir. Çeşitli çalışmalar, azo boyaların erkek reprodüktif sistemi üzerinde, özellikle de sperm parametrelerinde olumsuz etkileri olduğunu göstermiştir. Bu etkilere serum testosteron konsantrasyonundaki azalma da eşlik etmiştir.
Sonuç ve Tartışma: Gıda azo boyalarıyla ilgili çalışmalara olan ilginin artarak devam etmesi olası toksisite mekanizmalarını aydınlatma ihtiyacını beraberinde getirmiştir. Bu derlemede yaygın kullanılan gıda azo boyalarıyla ilgili genel bilgiler sunulmuş ve erkek reprodüktif sistem üzerindeki olumsuz etkilerine dair yapılan in vivo çalışmalar sonuçlarıyla değerlendirilmiştir.

Anahtar Kelimeler

Erkek reproduktif sistem, gıda azo boyaları, toksisite

Kaynakça

• 1. Burrows, J.D. (2009). Palette of our palates: A brief history of food coloring and its regulation. Comprehensive Reviews in Food Science and Food Safety, 8(4), 394-408. [CrossRef]
• 2. Zeece, M. (2020). Food colorants. In: M. Zeece (Ed.), Introduction to the Chemistry of Food, (pp. 313-344). Cambridge: Academic Press. [CrossRef]
• 3. Lehto, S., Buchweitz, M., Klimm, A., Straßburger, R., Bechtold, C., Ulberth, F. (2017). Comparison of food colour regulations in the EU and the US: A review of current provisions. Food Additives & Contaminants, 34(3), 335-355. [CrossRef]
• 4. Ramos-Souza, C., Bandoni, D.H., Bragotto, A.P.A., De Rosso, V.V. (2023). Risk assessment of azo dyes as food additives: Revision and discussion of data gaps toward their improvement. Comprehensive Reviews in Food Science and Food Safety, 22(1), 380-407. [CrossRef]
• 5. Majcen-Le Marechal, A., Slokar, Y.M., Taufer, T. (1997). Decoloration of chlorotriazine reactive azo dyes with H2O2/UV. Dyes and Pigments, 33(4), 281-298. [CrossRef]
• 6. Chequer, F.M.D., Dorta, D.J., de Oliveira, D.P. (2011). Azo dyes and their metabolites: Does the discharge of the azo dye into water bodies represent human and ecological risks. Advances in Treating Textile Effluent, 48, 28-48. [CrossRef]
• 7. Yamjala, K., Nainar, M.S., Ramisetti, N.R. (2016). Methods for the analysis of azo dyes employed in food industry-A review. Food Chemistry, 192, 813-824. [CrossRef]
• 8. König, J. (2015). Food colour additives of synthetic origin. In: M.J. Scotter (Ed.), Colour Additives for Foods and Beverages, (pp. 35-60). Woodhead Publishing. [CrossRef]
• 9. Cui, M.H., Liu, W.Z., Tang, Z.E., Cui, D. (2021). Recent advancements in azo dye decolorization in bio-electrochemical systems (BESs): Insights into decolorization mechanism and practical application. Water Research, 203, 117512. [CrossRef]
• 10. Hashemi, S.H., Kaykhaii, M. (2022). Azo dyes: Sources, occurrence, toxicity, sampling, analysis, and their removal methods. In: T. Dalu and N.T. Tavengwa (Eds.), Emerging Freshwater Pollutants, (pp. 267-287). Amsterdam: Elsevier. [CrossRef]
• 11. Kalia, A., Singh, S. (2020). Myco-decontamination of azo dyes: Nano-augmentation technologies. 3 Biotech, 10(9), 384. [CrossRef]
• 12. Mota, I.G.C., Neves, R.A.M.D., Nascimento, S.S.D.C., Maciel, B.L.L., Morais, A.H.D.A., Passos, T.S. (2023). Artificial dyes: Health risks and the need for revision of international regulations. Food Reviews International, 39(3), 1578-1593. [CrossRef]
• 13. Chung K.T. (2016). Azo dyes and human health: A review. Journal of Environmental Science and Health. Part C, Environmental Carcinogenesis & Ecotoxicology Reviews, 34(4), 233-261. [CrossRef]
• 14. Bafana, A., Devi, S.S., Chakrabarti, T. (2011). Azo dyes: Past, present and the future. Environmental Reviews, 19(NA), 350-371. [CrossRef]
• 15. Barciela, P., Perez-Vazquez, A., Prieto, M.A. (2023). Azo dyes in the food industry: Features, classification, toxicity, alternatives, and regulation. Food and Chemical Toxicology, 178, 113935. [CrossRef]
• 16. Cox, J.A., White, P.A. (2019). The mutagenic activity of select azo compounds in MutaMouse target tissues in vivo and primary hepatocytes in vitro. Mutation Research/ Genetic Toxicology and Environmental Mutagenesis, 844, 25-34. [CrossRef]
• 17. Josephy, P.D., Allen-Vercoe, E. (2023). Reductive metabolism of azo dyes and drugs: Toxicological implications. Food and Chemical Toxicology, 178, 113932. [CrossRef]
• 18. Amchova, P., Kotolova, H., Ruda-Kucerova, J. (2015). Health safety issues of synthetic food colorants. Regulatory Toxicology and Pharmacology, 73(3), 914-922. [CrossRef]
• 19. Fitch, S.E., Payne, L.E., van de Ligt, J.L.G., Doepker, C., Handu, D., Cohen, S.M., Anyangwe, N., Wikoff, D. (2021). Use of acceptable daily intake (ADI) as a health-based benchmark in nutrition research studies that consider the safety of low-calorie sweeteners (LCS): A systematic map. BMC Public Health, 21(1), 956. [CrossRef]
• 20. Dixit, S., Purshottam, S.K., Gupta, S.K., Khanna, S.K., Das, M. (2010). Usage pattern and exposure assessment of food colours in different age groups of consumers in the State of Uttar Pradesh, India. Food Additives & Contaminants, 27(2), 181-189. [CrossRef]
• 21. Mielech, A., Puścion-Jakubik, A., Socha, K. (2021). Assessment of the risk of contamination of food for infants and toddlers. Nutrients, 13(7), 2358. [CrossRef]
• 22. Reza, M.S.A., Hasan, M.M., Kamruzzaman, M., Hossain, M.I., Zubair, M.A., Bari, L., Abedin, M.Z., Reza, M.A., Khalid-Bin-Ferdaus, K.M., Haque, K.M.F., Islam, K., Ahmed, M.U., Hossain, M.K. (2019). Study of a common azo food dye in mice model: Toxicity reports and its relation to carcinogenicity. Food Science & Nutrition, 7(2), 667-677. [CrossRef]
• 23. Ameur, F.Z., Mehedi, N., Soler Rivas, C., Gonzalez, A., Kheroua, O., Saidi, D. (2019). Effect of tartrazine on digestive enzymatic activities: In vivo and in vitro studies. Toxicological Research, 36(2), 159-166.
• 24. Elbanna, K., Sarhan, O.M., Khider, M., Elmogy, M., Abulreesh, H.H., Shaaban, M.R. (2017). Microbiological, histological, and biochemical evidence for the adverse effects of food azo dyes on rats. Journal of Food and Drug Analysis, 25(3), 667-680. [CrossRef]
• 25. Atlı Şekeroğlu, Z., Güneş, B., Kontaş Yedier, S., Şekeroğlu, V., Aydın, B. (2017). Effects of tartrazine on proliferation and genetic damage in human lymphocytes. Toxicology Mechanisms and Methods, 27(5), 370-375. [CrossRef]
• 26. Kızıltan, T., Baran, A., Kankaynar, M., Şenol, O., Sulukan, E., Yıldırım, S., Ceyhun, S.B. (2022). Effects of the food colorant carmoisine on zebrafish embryos at a wide range of concentrations. Archives of Toxicology, 96(4), 1089-1099. [CrossRef]
• 27. Bezerra, M.D.S., Malaquias, G.D.S., Castro E Sousa, J.M.D., Peron, A.P. (2016). Cytotoxic and genotoxic potential of powdered juices. Food Science and Technology, 36, 49-55. [CrossRef]
• 28. Pérez-Ibarbia, L., Majdanski, T., Schubert, S., Windhab, N., Schubert, U.S. (2016). Safety and regulatory review of dyes commonly used as excipients in pharmaceutical and nutraceutical applications. European Journal of Pharmaceutical Sciences, 93, 264-273. [CrossRef]
• 29. Alshehrei, F. (2020). Role of microorganisms in biodegradation of food additive dyes: A review. African Journal of Biotechnology, 19(11), 799-805. [CrossRef]
• 30. Boussada, M., Lamine, J.A., Bini, I., Abidi, N., Lasrem, M., El-Fazaa, S., El-Golli, N. (2017). Assessment of a sub-chronic consumption of tartrazine (E102) on sperm and oxidative stress features in Wistar rat. International Food Research Journal, 24(4), 1473-1481.
• 31. Mohamed Hosieny, N., Ibrahim, M.E.-D., Ahmed, S.M., Mohammad Hassan, M.Z. (2022). Potential protective role of curcumin on the toxic effect of food azo dye tartrazine on the brain of young albino rats. Toxicology International (Formerly Indian Journal of Toxicology), 29(1), 15-32. [CrossRef]
• 32. Biswas, P., Jain, J., Hasan, W., Bose, D., Yadav, R.S. (2023). Azo food dye neurotoxicity in rats: A neurobehavioral, biochemical, and histopathological study. Food and Chemical Toxicology, 181, 114067. [CrossRef]
• 33. Saxena, B., Sharma, S. (2015). Food color induced hepatotoxicity in Swiss albino rats, Rattus norvegicus. Toxicology International, 22(1), 152-157. [CrossRef]
• 34. Ibrahim, A.A., El-Sherbeny, A.S., Al-Shaikh, T.M. (2020). Prophylactic effect of vitamin E on carmoisine food dye induced kidney damage in male mice: Histological, physiological and immunological studies. Applied Biological Research, 22(1), 34-45. [CrossRef]
• 35. Amin, K.A., Hameid, H.A. II, Elsttar, A.A. (2010). Effect of food azo dyes tartrazine and carmoisine on biochemical parameters related to renal, hepatic function and oxidative stress biomarkers in young male rats. Food and Chemical Toxicology, 48(10), 2994-2999. [CrossRef]
• 36. Khayyat, L., Essawy, A., Sorour, J., Soffar, A. (2017). Tartrazine induces structural and functional aberrations and genotoxic effects in vivo. PeerJ, 5, e3041.
• 37. Mehedi, N., Ainad-Tabet, S., Mokrane, N., Addou, S., Zaoui, C., Kheroua, O., Saidi, D. (2009). Reproductive toxicology of tartrazine (FD and C Yellow No. 5) in Swiss albino mice. American Journal of Pharmacology and Toxicology, 4(4), 130-135. [CrossRef]
• 38. Chatterjee, P., Alvi, M.M. (2014). Excipients and active pharmaceutical ingredients. In: D. Bar-Shalom and R. Klaus (Eds.), Pediatric Formulations: A Roadmap, (pp. 347-361). New York: Springer.
• 39. Gultekin, F., Doguc, D.K. (2013). Allergic and immunologic reactions to food additives. Clinical Reviews in Allergy & Immunology, 45(1), 6-29.
• 40. Elekima, I., Nwachuku, O.E., Ukwukwu, D., Nwanjo, H.U., Nduka, N. (2019). Biochemical and histological changes associated with azo food dye (tartrazine) in male albino rats. Asian Journal of Research in Biochemistry, 5(1), 1-14. [CrossRef]
• 41. Demirkol, O., Zhang, X., Ercal, N. (2012). Oxidative effects of tartrazine (cas no. 1934-21-0) and new coccin (cas no. 2611-82-7) azo dyes on CHO cells. Journal für Verbraucherschutz und Lebensmittelsicherheit, 7, 229-236.
• 42. Meghapriya, A., Kishori, B. (2019). Tartrazine, a male reproductive supressor in adult albino rats. International Journal of Life Sciences Research, 7(3), 1-10.
• 43. Becker, S., Berhane, K. (1997). A meta-analysis of 61 sperm count studies revisited. Fertility and Sterility, 67(6), 1103-1108. [CrossRef]
• 44. Hirsh A. (2003). Male subfertility. British Medical Journal, 327(7416), 669-672. [CrossRef]
• 45. Brugh, V.M., Lipshultz, L.I. (2004). Male factor infertility: Evaluation and management. The Medical Clinics of North America, 88(2), 367-385. [CrossRef]
• 46. Gautam, D., Sharma, G., Goyal, R. P. (2010). Evaluation of toxic impact of tartrazine on male Swiss albino mice. Pharmacologyonline, 1, 133-140.
• 47. Meena, G., Meena, B. (2020). Evaluation of possible toxic effect of tartrazine food dye on wiss albino mice, and histology of testis. International Journal For Innovative Research In Multidisciplinary Field, 6(7), 100-105.
• 48. Ara, C., Arshad, A., Faheem, M., Khan, M., Shakir, H. A. (2022). Protective potential of aqueous extract of Allium cepa against tartrazine induced reproductive toxicity. Pakistan Veterinary Journal, 42(3), 358-363.
• 49. Khatun, A., Nath, P.P., Mondal, M., Pal, S., Paul, G. (2022). Suppression of male reproductive function by Brown HT in rat. Asian Journal of Pharmaceutical and Clinical Research, 15(5), 76-82. [CrossRef]
• 50. Ismail, M.A. (2016). Molecular and cytochemical comparative assessment between the two food additives, sunset yellow and curcumin-induce testicular toxicity in mice. Journal of Bioscience and Applied Research, 2(7), 509-523. [CrossRef]
• 51. Mathur, N., Chowdhary, V., Mehta, M., Krishnatrey, R. (2005). Effect of sunset yellow on testis in rats. Journal of Ecophysiology and Occupational Health, 5(1), 1-3.
• 52. Ramm, S.A., Stockley, P. (2010). Sperm competition and sperm length influence the rate of mammalian spermatogenesis. Biology Letters, 6(2), 219-221. [CrossRef]
• 53. O'Donnell, L., Stanton, P., de Kretser, D.M. (2015). Endocrinology of the male reproductive system and spermatogenesis. In: R. McLachlan (Ed.), Endocrinology of the Male Reproductive System, (pp 1-57). South Dartmouth: MA.
• 54. Moutard, L., Goudin, C., Jaeger, C., Duparc, C., Louiset, E., Pereira, T., Fraissinet, F., Delessard, M., Saulnier, J., Rives-Feraille, A., Delalande, C., Lefebvre, H., Rives, N., Dumont, L., Rondanino, C. (2023). Steroidogenesis and androgen/estrogen signaling pathways are altered in in vitro matured testicular tissues of prepubertal mice. eLife, 12, RP85562. [CrossRef]
• 55. Elekima, I., Nwachuku, O.E. (2019). Evaluation of acute and chronic toxicity of tartrazine (E102) on steriod reproductive hormones of albino rats. Asian Journal of Research and Reports in Endocrinology, 1-15. [CrossRef]
• 56. Elewa, Y.H.A., Mohamed, A A., Galal, A.A.A., El-Naseery, N.I., Ichii, O., Kon, Y. (2019). Food Yellow4 reprotoxicity in relation to localization of DMC1 and apoptosis in rat testes: Roles of royal jelly and cod liver oil. Ecotoxicology and Environmental Safety, 169, 696-706. [CrossRef]
• 57. Khiralla, G., Salem, S., El-Malky, W. (2015). Effect of natural and synthetic food coloring agents on the balance of some hormones in rats. International Journal of Food Science and Nutrition Engineering, 5(2), 88-95.
• 58. Alsudani, A.A., Alhamadawi, H.A. (2020). A physiological study of the effect of some food additives on the hypothalamic-pituitary-testis axis in male albino rats. In Journal of Physics: Conference Series, 1664(1), 012122. [CrossRef]
• 59. Abbas, J. R., AlHamadawi, H. A. (2019). Effect of chocolate brown HT E155 on some hormones in male albino rats. EurAsian Journal of BioSciences, 13(1), 485-489.
• 60. Mahmoud, N. H. (2006). Toxic effects of the synthetic food dye brilliant blue on liver, kidney and testes functions in rats. Journal of the Egyptian Society of Toxicology, 34(4), 77-84.
• 61. Wopara, I., Modo, E. U., Mobisson, S. K., Olusegun, G. A., Umoren, E. B., Orji, B. O., Mounmbegna, P. E., Ujunwa, S. O. (2021). Synthetic Food dyes cause testicular damage via up-regulation of pro-inflammatory cytokines and down-regulation of FSH-R and TESK-1 gene expression. JBRA Assisted Reproduction, 25(3), 341-348. [CrossRef]
• 62. Moutinho, I.L., Bertges, L.C., Assis, R.V. (2007). Prolonged use of the food dye tartrazine (FD&C yellow no 5) and its effects on the gastric mucosa of Wistar rats. Brazilian Journal of Biology, 67(1), 141-145. [CrossRef]
• 63. Rehman, K., Ashraf, A., Azam, F., Akash, M.S.H. (2019). Effect of food azo-dye tartrazine on physiological functions of pancreas and glucose homeostasis. Turkish Journal of Biochemistry, 44(2), 197-206. [CrossRef]
• 64. Visweswaran, B., Krishnamoorthy, G. (2012). Oxidative stress by tartrazine in the testis of Wistar rats. Journal of Pharmacy and Biological Sciences, 2(3), 44-49.
• 65. Fanaei, H., Khayat, S., Halvaei, I., Ramezani, V., Azizi, Y., Kasaeian, A., Mardaneh, J., Parvizi, M.R., Akrami, M. (2014). Effects of ascorbic acid on sperm motility, viability, acrosome reaction and DNA integrity in teratozoospermic samples. Iranian Journal of Reproductive Medicine, 12(2), 103-110.
• 66. Giribabu, N., Kumar, K. E., Rekha, S. S., Muniandy, S., Salleh, N. (2014). Chlorophytum borivilianum (Safed Musli) root extract prevents impairment in characteristics and elevation of oxidative stress in sperm of streptozotocin-induced adult male diabetic Wistar rats. BMC Complementary and Alternative Medicine, 14, 291.
• 67. Vernet, P., Fulton, N., Wallace, C., Aitken, R.J. (2001). Analysis of reactive oxygen species generating systems in rat epididymal spermatozoa. Biology of Reproduction, 65(4), 1102-1113. [CrossRef]
• 68. Ruiz-Valderrama, L., Posadas-Rodríguez, J., Bonilla-Jaime, H., Tarragó-Castellanos, M.D.R., González-Márquez, H., Arrieta-Cruz, I., González-Núñez, L., Salame-Méndez, A., Rodríguez-Tobón, A., Morales-Méndez, J.G., Arenas-Ríos, E. (2022). Sperm dysfunction in the testes and epididymides due to overweight and obesity is not caused by oxidative stress. International Journal of Endocrinology, 2022, 3734572. [CrossRef]
• 69. Maciejewski, R., Radzikowska-Büchner, E., Flieger, W., Kulczycka, K., Baj, J., Forma, A., Flieger, J. (2022). An overview of essential microelements and common metallic nanoparticles and their effects on male fertility. International Journal of Environmental Research and Public Health, 19(17), 11066. [CrossRef]
• 70. Chinnaiyan, A.M., Orth, K., O'Rourke, K., Duan, H., Poirier, G.G., Dixit, V.M. (1996). Molecular ordering of the cell death pathway. Bcl-2 and Bcl-xL function upstream of the CED-3-like apoptotic proteases. The Journal of Biological Chemistry, 271(9), 4573-4576.
• 71. Suzuki, T., Onogawa, T., Asano, N., Mizutamari, H., Mikkaichi, T., Tanemoto, M., Abe, M., Satoh, F., Unno, M., Nunoki, K., Suzuki, M., Hishinuma, T., Goto, J., Shimosegawa, T., Matsuno, S., Ito, S., Abe, T. (2003). Identification and characterization of novel rat and human gonad-specific organic anion transporters. Molecular Endocrinology, 17(7), 1203-1215. [CrossRef]
• 72. Mahfouz, M.E., Moussa, E.A. (2015). The impact of curcumin administration on the food colouring Sunset Yellow‐induced damage in testes and liver of male rat: gene expression and ultrastructural studies. Egyptian Journal of Expert Biology (Zoology), 11, 43-60.
• 73. Montaser, M., Abiya, R.A., Afifi, M., Saddick, S., Allogmani, A.S., Almaghrabi, O.A. (2018). Effect of natural and synthetic food colorants on spermatogenesis and the expression of its controlling genes. Veterinary Medicine in-between Health & Economy (VMHE), 55.
• 74. Niemi, M., Kormano, M. (1965). Cyclial changes and significance of lipids and acid phosphatase hydrolysis in the seminiferous tubules of the rat testis. Anatomical Record, 12, 131-150. [CrossRef]